CFS-A IR M-42
Not for publication
ECOLOGY OFMULSANTINA HUDSONICA CASEY,A LADYBEETLE IN FIR-SPRUCEFOREST
$1
by
I. W. VartyMAR 27 1989
DEPT. OF FORESTRYFREDERICTON N.B.
FOREST RESEARCH LABORATORYFREDERICTON, NEW BRUNSWICK
INTERNAL REPORT M-42
FORESTRY BRANCHDEPARTMENT OF FISHERIES AND FORESTRY
JANUARY, 1969
CANADA
Department of Fisheries and Forestry
ECOLOGY OF MULSANTINA HUDSONICA CASEY,
A LADYBEETLE IN FIR-SPRUCE FOREST
by
I. W. Varty
Forest Research Laboratory
Fredericton, New Brunswick
Internal Report M-42
Forestry BranchJanuary, 1969
(This report may not be published in whole or in part without thewritten consent of the'Regional Director, Maritimes, Department ofFisheries and Forestry, P. O. Box 4000, Fredericton, N. B.)
TABLE OF CONTENTS
INTRODUCTION . . 0 . 9 0* OOO * 0 9 • 0 0 9 ** 0 *
METHODS . . 0 o • 0 0 9 0 0 0 0* 0 0 0 9 • • • 0 0 0 0 0 0 0
-Laboratory rear ings 000000 ** 00 *** 0■004•0
Page
1
1-Field temperature records 0 2-Field sampling . 0 . , . 0 . . . . . 0 2-Location of sample plots 3
DESCRIPTION . . • • 9 0 ■ 0 4
-Adult 0•00•000009•0 OOOOOOO 0. OOOO 9 4-Immature stages . . . ..... OOO *0 O 0000•000 5
SEASONAL HISTORY . . . . ■ 000 O .. OOOO *0000000 0 5
-Seasonal development 5-Habitat . 8
FOOD ECOLOGY . . . . . OOOO . . . . O . 9
-The main prey species . 9-Food specificity of adults 9-Food specificity of larvae 10-Daily activity of adults 11-Seasonal voracity of adults 13-Voracity of larvae 15-Relationship between food intake by larvaeand subsequent size of adults ......... * 0 0 0 00 17
-Other coccinellid species on fir 19
POPULATION RELATIONSHIPS BETWEEN MULSANTINA HUDSONICAAND MINDARUS ABIETINUS 19
-Synchronism of life cycles and comparisonof population densities 19
-The effect of insecticides on prey-predatorrelationships 22
-A comment on sampling problems . . . . a .. • 9 . . . 24
DISCUSSION . . .000 ... ■ ...... * 6000000000 25
SUMMARY .• 26
INTRODUCTION
The perennially reliable source of prey biomass in balsam firfoliage in most parts of the Maritime Provinces is the balsam twigiaphid, Mindarus abietinus Koch. This aphid is usually abundant fromMay to July, and offers a food niche for many species of predators whichseek or tolerate the fir habitat. One of the predators most constantlyassociated with the aphid is the ladybeetle Mulsantina hudsonica Casey.A study of this ladybeetle is in progress to determine; (1) its role inthe community ecology of fir-infesting arthropods; (2) its influenceen populations of the spruce budworm, Ohoristoneura fumiferana (Olen.);and (3) the effect of insecticides (used against the budworm) upon lady-beetle survival and upon the ladybeetle-aphid interaction. The approachto these problems has been through a study of the ladybeetle's seasonalhistory and food ecology and by comparing population dens it ies of bothpredator and prey in the field.
METHODS
Laboratory rearings
Laboratory studies of the development and voracity of M. hudsonica were conducted at Fredericton, N. Ba, in 1967 and 1968. The ladybeetleadults and the balsam twig aphids w collected at random in the field.
Adult and immature beetles were reared individually on shoots ofbalsam fir within half-pint plastic containers. Each container had a falsefloor of paraffin wax sealing a water reservoir into which the cut shootswere inserted, it was also tapped by a cotton wick as a drinking supplyfor the ladybeetles. The container was capped by a nylon mesh.
Ladybeetles were fed on live and frozen aphids, and on twoartificial diets modified from those prepared by Smith (1965). These diets(per 100 gm) were as follows:
1. Difco beef extract peptone 40 gm, sucrose 54 gm, cholesterol0.3 gm, salt 1.5 gm, RNA 1,5 gm, wheat germ 2.0 gm, cholinechloride 0.1 gm, inositol chloride 0.1 gm, and 0.1 gm B vitaminmixture (niacinamide 50 mg, calcium pantothenate 25 mg , thiaminhydrochloride 16 mg, riboflavin 12 mg; pyridoxine hydrochloride12 mg, folic acid 1 mg, biotin 0,2 mg, B 12 0.02 mg). As thispreparation was deliquescent, it was kept in a stoppered bottleunder refrigeration.
2. As above but substitute Brewer's Yeast Powder for Difco beefextract peptone. This was also kept dry and refrigerated,
The ladybeetles were reared either in controlled environmentalchambers' or on the insectary beaches. In the former, the temperatureregimes established were (1) 7 F for a 16-hr period under fluorescentlamps alternating with 60 F for an 8-hr period in darkness (2) 70/60 F(3) 65/60 F (4) 60 F constant. Thus three regimes had a diurnal temperature
- 2:
fluctuation, and all regimes had the same long photoperiod. Thealternation of warmth and coolness was programmed because high constanttemperatures have been shown to depress ladybeetle feeding and ovipositionalresponses (Way, 1966). Humidity was uncontrolled but high due to themoist wick and transpiring foliage in each cage.
At the insectary benches, temperatures were uncontrolled butcorresponded closely to shade temperatures out-of-doorsa Natural lightwas used but cages were shaded from direct insolation.
Field temperature records
Temperatures were recorded in Stevenson Screens close to eachplot. Degree-day graphs of accumulated effective heat-units were preparedto compare the varying seasonal heat inflow in different plots and differentyears (Fig. 7). The degree-day value over base 42 F for each day wascalculated from a sine curve relationship between maximum and minimumreadings, as computed by Dr. R. F. Morris of this laboratory. The use ofaccumulated degree-days permitted between-plot and between-year comparisonof ladybeetle population development concurrently with aphid populationdevelopment.
The degree-day concept is also useful in relating the rate ofinsect development in the laboratory to the rate in the field. However,degree-day values in the field are based on shade temperatures andgenerally underestimate the real heat inflow in microhabitats subject todirect insolation. Although degree-day values for a controlled environmentare measured exactly, rates of development in the field tend to be somewhatfaster than anticipated from laboratory rearings.
Field sampling
The sampling method (Varty, 1968) was designed primarily forstudy of aphid distribution in fir; but since collection of the fauna iscomprehensive, the method also yields information on comparative densitiesof prey and predators in plots with differing ecological backgrounds (standcharacters, climate, insecticide history). For study of the verticaldistribution of insects within a tree, the crown is arbitrarily dividedinto four portions (of equal length along the axis) designated A, B, Cand D from the top downwards (Morris,1955). Since earlier studies ofM. abietinus showed that B-level samples gave an acceptable index of whole-tree populations one B-level branch was collected from each of 40 treesper plot per date in 1966 and 1967. The surface area of each branch wasmeasured as the product of foliar length and mean width. The branch wasthen clipped into convenient lengths and stored with all its arthropods,including those which dropped to the canvas, in a 1 quart Mason jar of60% alcohol. Later the fauna was separated from the vegetation by 'ascreening and vacuum filter process (Varty, 1968).
The suitability of B-level sampling for coccinellids remainsuntested. The method of collection does not yield an accurate estimateof adult populations because of the adult flight response, and because of
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changing diurnal and seasonal habitats. However, the method efficientfor measuring and comparing coccinellid larval populations with thoseof associated aphids.
No satisfactory index of adult density is yet available, However,a comparison of adult abundance in two plots was obtained by a beatingprocedure. At each sampling date, approximately 400 ft - of D-Level branchsurface from several trees picked at random were beaten in situ over acanvas. The ladybeetles were then counted and released. This procedurewas undertaken only in the afternoons when ladybeetle activity on thefoliage was at peak, i. e. the minimal number of adults would be concealedin places from which dislodgement would be improbable. These talliesgauge adult ladybeetle abundance on D-level branches across the season,but they do not offer an index of whole tree populations, or provide anequable measure of population abundance across the season, They are usefulfor gross comparisons of static populations, i.e. comparisons between hosttree species within one plot at one date, or comparisons between plots whendegree-day accumulations can be equated and weather conditions are similar.
Location of sample plots
The locations of sample plots were
Lincoln, Sunbury Co., N. B. 1966, 1967Killarney, York Co., N. B. 1966Penniac, York Co., N. B. 1966, 1967Green River, Madawaska Co., N. B. 1967Priceville, Northumberland Co., N. B. 1967.
Plots were chosen in similar stands of pole-stage, even-sizedbalsam fir with as much homogeneity of ecological condition as possible.Each plot consisted of 40 codominant trees, all 30 to 35 feet high, sothat B-level was within the range of pole clippers. The chief associatedtrees in all plots were red spruce, white birch, and red maple.
The data from the Lincoln plot were used as the criterion of"'normal" community relationships because the stand had no recent historyof budworm outbreak, logging, or insecticide treatment. Moreover, itoccurs in the phonological zone of greatest summer warmth within theprovince of New Brunswick.
The Killarney plot was treated with DDT for the first e in1966; it was aerially sprayed with 0,25 lb. DDT in 0.5 gal (U.S.) oilformulation per acre first at 400 degree-days (henceforth D) on 1 June,then again at 550 D (10 June) Killarney sustained light budworm infest-ations in 1965 and in 1966, but there was no noteworthy defoliation.
The Penniac plot was aerially sprayed with an organophosphorouscompound in 1966, the only year of insecticide application. The dosagewas 0.25 lb. Phosphamidon in 0.5 gal (U.S.) water formulation per acreat each of two applications-370 D (1 June) and 590 D (14 June).
Penniac suffered light defoliation by the spruce budworm 1966, butthere was a marked recovery and no noteworthy defoliation. in 1967. BothPenniac and Killarney lie within the same phonological zone as Lincoln,all three are close to Fredericton, N. B.
The Green River plot (G 17) was chosen to see what effect ashorter cooler growing season might have on the development of prey andpredator, populations. The plot has no recent history of insecticideapplication or budworm attack.
The Priceville plot in the Miramichi catchment area was selectedbecause it has had a perennial history of DDT application since 1957,totalling 4.5 lb./acre in the decade, and a continuing budworm infestationor hazard. In the year of sampling, 1967, DDT was applied in two lotsof 0.25 lb./acre at 430 D (16 June) and at 510 D (20 June) Budwormdefoliation in that year was light to moderate.
DESCRIPTION
Adult
Mulsantina hudsonica, described in detail by Hatch (1962) isa small shiny brown ladybeetle with black markings (Fig. la). The groundcolour of the elytra varies among individuals from a pale yellow brownto a fuscous brown. The pronotum is always paler. The dimensions ofbody size and weight (Table 1) show that overwintered female adults area little heavier than males but approximately the same size. In otherarboreal species in Canada measured by Smith (1966) the females aremarkedly larger than the males.
Table 1. Size and Weight of Adults and Larvae of Mulsantina hudsonica
ADULTS
Measurement Male Female
Mean Range Mean Range
Body length (mm) 4.43 4.15-4.86 4.45 4.12-4.88Head width (mm) 1.25 1.20-1.32 1.25 1.12-102Live weight (mg) 7.01 4.90-8.40 8.23 4.80-11.60
18 22
LARVAE
Measurement
Body length (mm) 1.93 3.53 4.67 6.42Head width (inn) .42 .52 .68 .84Live weight (mg) .26 1.48 3.15 8,38Freeze-dry weight (mg) .11 .39 .93 3.70No, specimens 21 6 5 13
No. specimens,
a Adults weighed in early une 196$ at beginning ofwhen weight is maximal.
reproductive period,
Figure 1. Mulsantina hudsonica Casey : (A) adult, (B) fourth-instar larva,(C) pupa, (0) egg mass; one larva had emerged and fed upon threeother eggs; dark eggs contain larvae ready to emerge.
5
Immature stages
The egg (Fig. 1d) elongate, bluntly rounded ends; length1.5 mm, maximum diameter 0.6 mm; surface minutely and irregularlyspinulate. Bright yellow when fresh, darkening as the embryo develops,
The ultimate instar (fourth) larva (Fig. lb, Table 1): fusiform,widest at metathorax; light grey with darker intersegmental patches and darkgrey verrucal plates. Head slightly wider than long, sides subparallel;dorsum with distinct epicranial suture. Head with many fine setae, notlonger than 4 width of head. Antenna 2-segmented, small and dark.Mouthparts hypognathous; mandible falcate, bidentate at apex. Maxillatriangular, dark; maxillary palp short, tapering, truncate and 3-segmented.Labium soft, pale, with palpi 2-segmented. Three ocelli posterior toeach antenna. Pronotum elliptical, l times wider than long, bearing twolarge sclerotized areas adjoining along the median line; rimmed with setae.Meso- and meta-terga about twice as Wide as long, each with a dark setiferousand spinous area on each side widely separated; conspicuous spiracle oneach side of mesotergum. Legs setaceous, each tibia tipped with abundanttenent hairs and a minute tarsungulus. Abdominal segments 1-8 eachequipped with 4 dark setiferous and spinous areas arranged transverselyalong tergum; an annular spiracle on each side; pleuron pale grey witha setiferous area, ventrum pale with segmental rows of verrucae. Segment9 setiferous gong posterior rim. Segment 10 eversible as an analsucking disc. 'Dusky patches coalescent over most abdominal tergites,contrasting with darker spines and pale pleural stripe.
Pupa (Fig. 1c): larval exuviae present at point of anal attachmentto foliage. Head not attached to substrate. Dorsum grey white, with elytragrey, and various dark grey patches laterally on tergites of thorax and mostabdominal segments.
SEASONAL HISTORY
Seasonal development
Mulsantina hudsonica has evolved a strictly univoltine cyclein New Brunswick, based on a short spring season of prey abundance, ashort hot summer, and a long cold winter. The following sequence ofevents refers to seasonal behaviour at Fredericton, 1966 to 1968.
Adults of both sexes emerged from their overwintering sitesaround the beginning of May. Thereafter adults were found on the foliagein warm periods of the day with increasing frequency. In cool periods ofthe day, they apparently concealed themselves elsewhere than on thefoliage.
The sex ratio of overwintered adults is not known, but it maywell vary from year to year. In May 1968, a collection of 50 adultsmade in a single stand contained 17 males and 33 females. CopulationOf caged pairs was obersved from mid-May to mid-June, most pairs matedseveral times at irregular intervals of one to several days.
6
The interval between first mating and oviposition was around eightdays, and oviposition began in late May. Eggs were laid in clusters of 2to 10 eggs, but usually 8, at intervals of 2 to 6 days over an ovipositionperiod of about 20 days. Five caged individuals had fecundities of 38,32, 32, 31, and 14 eggs; this is a very low fecundity compared with othercoccinellid species reported in the literature. Eggs were laid in thevicinity of the prey in nature, but in cages, large or small, they werefrequently laid on woodwork or screening remote from the food source.The low fecundity and short ovipositional season may have evolved in responseto the brief seasonal abundance of the balsam twig aphid. The possibilityof a numerical response in oviposition, 1 e. an adjustment of the rate ofoviposition to the seasonal and local abundance of prey, has not yet beenexplored.
Egg incubation at field temperatures in June was 7 to 11 days, andhatching took place from mid-June to early July. Hatching was observedrepeatedly during the warm hours of each day but it is not known whetherany diurnal rhythm operates in response to temperature threshold or timeof day. Hatching was usually closely synchronized within each cluster.Larvae frequently remained at the egg cluster for the first day, but there-after dispersed and maintained no association with siblings.
There are four larval stadia. The first three were 3 to 4 dayseach, and the fourth about 7 days, around 18 days in all, in rearings atquasi-natural temperatures, mean 67 F, in the insectary. However, the rateof development increases with temperature, so in general early hatchinglarvae tend to develop more slowly than late hatching individuals. Incubatorrearings showed that the degree-days required for completion of larvaldevelopment remained fairly constant around 475 but stadia length in daysdecreased with warmer regimes (Table 2).
The larvae of all instars foraged among the foliage throughoutthe warm part of the day except when fully fed or about to moult. Thisactivity appeared as a random movement among the shoots, alternating witha more vigorous searching after contact with Prey. All instars used thesticky anal disc when walking, feeding, resting or moulting. Larvaewere not seen after the third week of July.
Pupation required about 8 days, with little variation at prevailinginsectary temperatures, and occurred during July or rarely in earlyAugust. The pupa was affixed to the shoot by the anal secretion and respondedto touch by a vigorous rocking on this pivot.
Adults of the new generation appeared as early as 10 July, andmatured as late as early August.
Teneral adults foraged vigorously in the first week but graduallyentered a state of partial quiescence, concealing themselves under barkor other shaded damp niches during August to October. They sheltered insmall temporary aggregations, resuming activity on the foliage from timeto time. Presumably this resumption was for food and drink, but gutdissections of adults in late summer have shown little evidence of solidfood consumption,
7
Table 2. Rate of Development in Days and Degree-Days of Larvae ofMulsantina hudsonica in Various Temperature Regimes
(Mean of 3 Larvae/Regime)
Regime(day/night)
InstarTotalII III V
Days
60 const. 4.0 4.2 6.2 11.8 22.265/60 F 4.0 4.0 5.0 11.0 20.070/60 F 4.0 3.0 4.0 8.7 15.775/60 F 3.0 3,0 3.5 8.7 15.2
Degree-Days
60 const. 72 76 112 212 47265/60 F 80 80 100 2:20 48070/60 F 92 69 92 200 45375/60 F 78 78 91 226 473
Adults display the death-feigning habit and reflex bleedingon severe disturbance, in common with other coccinellids, but this doesnot deter woodpeckers from seeking the concealed adults as food.
From October, the adults settled in hibernation sites whichhave not yet been discovered, but which are presumably at or near thesurface of the forest floor. There was no evidence of migration orchange of habitat prior to hibernation. Attempts to induce aggregationsby use of attractants (captive adults, or the sex attractant octodecanitrile)were unsuccessful. In other ladybeetles, large overwintering aggregationsserve to bring the sexes together for mating prior to spring dispersal(Hagen, 1962). M. hudsonica has no such need because it does not migrateto new habitats.
Adults of both sexes and both generations (the current year'sand the previous years) entered hibernation, but it is not knownwhether old adults successfully survive a second winter. The evidencefrom other species in Canada suggests that a second reproductive yearis feasible (Putman, 1955; Smith, 1965).
The larvae of a hymenopterous parasite, presumably a singlespecies, were observed frequently in dissections of male and femaleadult digestive tracts in fall and in spring. Only one parasite perhost was found, and it was located in the fat tissues around theoesophagus or mid-intestine. Adult parasites have not been reared,but they presumably emerge in spring.
8
Habitat
Mulsantina hudsonica has a narrow range of ecological habitat,although it is distributed across the-North American continent. InNew Brunswick, Immature stages of this ladybeetle have been found onlyin the spruce-fir ecosystem. However, adults have been collected fromred, white, and black spruces; balsam fir; red, White , and jack pines;tamarack; apple; wire and white birches; and aspen. The spruces andbalsam fir are the main hosts for all stages.
Sampling for adults by beating in the' Lincoln (unsprayed) and.Priceville (perennial DDT) showed a trend in change of preference betweenfir and red spruce across the season (Table 3). There was an early-seasonpreference for balsam fir, but a tendency to change to spruce in the lateovipositional period, and a clear preference for spruce inthe summer periodof quiescence. The early preference for fir is undoubtedly due to theabundance and rapid development of Mindarus abietinus. The related aphidon spruce, M. obliquus Cholodkovsky hatches 7 to-10 days later, so ifladybeetle oviposition is prey density-dependent, spruce may become attractiverather tardily. The low counts of adults from July onwards are an expressionof reduced activity on the foliage, not of reduced absolute populations.The tallies show somewhat similar densities for each plot in spite of theuse of insecticide in one. The comparative densities of larval ladybeetleson the various species of spruce and on balsam fir have not been investigated.
On balsam fir, adults and larvae have been collected at all levelswithin the crown. However, since aphid populations are densest in the D-levelat the time of oviposition, it is possible, but has not been tested, thatladybeetle larval density may be greatest in the lower crown.
Table 3. Tallies of Mulsantina hudsonica Adults Collected from 400 ft2Branch Surface by a Standard Beating Procedure from Two Plots-1967
Date Lincoln (unsprayed) Date Priceville (sprayed)
Balsam fir Red spruce Balsam fir Red spruce
8 June 37 14 9 June 126 4015 June 119 43 16 June 30 . 3820" June 5 2928 June 16 ' 513 Jay 2 2, 11 July 6 619 July 2 1 20 July 1 127 July 1 73 Aug. 1 16
11 Aug. 0 1224 Aug. 0 4 17 Aug. 1 71 Sept. 0 • 4 14 Sept. 3 2
FOOD ECOLOGY
The numbers and distribution of M. hudsonica are subject to theavailability of acceptable growth-promoting foods at a sufficient densityand over a sufficient period of time in the spruce-fir forest. Food ecologyis the study of (1) the identification of foods and the determination ofquantities; (2) the effects of foods on ladybeetle distribution, reproduct-ivity, and immature development; and (3) ladybeetle behaviour relative to food.
The main prey species
Field observations and laboratory experiments have demonstrated thatthe aphid'M. abietinus is the main prey for adults and larvae of M. hudsonica on balsam fir. However, this aphid is itself variable in size (Varty, 1968)and in weight (Table 4) according to generation and instar. The first gen-eration developing from overwintered eggs is termed the stem mother. Thishas four nymphal instars, and becomes an adult of middle size and weight.Its live-born offspring are females of two kinds, the abundant sexuparae(alates) and the relatively scarce fundatrigeniae (non-winged). Both formsbecome adults after four nymphal instars, and are relatively large aphids.The offspring of the fundatrigeniae are always sexuparae.' The offspring ofsexuparae, whether born of stem mothers or fundatrigeniae, are sexualswingless males and females with 1:1 sex ratio. The male is a dwarf non-feeding morph, and the female sexual (ovipara) is also small and short-lived.Thus, looked upon as a food supply, both aphid numbers (frequency of contacts)and weight of the individual (satisfaction of hunger) are important. Theseasonal abundance of the aphid can be expressed as density in numbers oras density in biomass (Fig. 3), but the latter is preferable in predatoryrelationships.
The other major prey species is Cinara abieticola (Choi.). Thisis a much larger aphid occurring in colonial groups on foliage at all crownlevels. It is 'usually much less abundant in terms of numbers and much morespotty in distribution in space and time. Its population dynamics andsuccession of igeneratons are unknown.,
Table 4. Mean Live Weight (in mg) of Mindarus abietinus by Instar andGeneration (Number of Specimens Measured ̀in Parentheses)
GenerationInstar Adult
II III IV
Stem mother O.015(211) 0.044(100) 0.101(110) 0.217(65) 0.373(45)Sexupara .024(250) 4)91(165) .296(100 ) .534(100) .452(100)Fundatrigenia .270(x) .420(20)Male .017(130) .014(200) .014(213) .010(200)Ovipara .024(246) .035(60) .038(100) .034(100)
FoodThe adult choice of prey in the field was determined by dissection
of some 60 adults and examination of the oesophagus mounted in HoyertsMedium. Ladybeetles for dissection were collected in the afternoon when most
10
feeding takes place, from April to September. The large proportion ofspecimens with no identifiable gut contents confirms the rearing observationthat adults feed discontinuously with long intervals between meals.
Mindarus and Cinara stem mothers were found in the tracts ofMulsantina within 2 weeks of the emergence of these ladybeetles fromhibernation sites, and both aphids were again the main diet during theladybeetle's reproductive phase. Other unidentified insect fragments wereoccasionally found, and vegetable fragments were not infrequent—fungalthreads, spores, and conifer pollen. In summer, the digestive tracts ofadults of the generation were uniformly empty after August, except for oneindividual with mineral fragments.
In cage experiments, adults readily accepted spruce budworm eggsand first-instar larvae in July, and second-instars in May. Variousappendages (mandibles, prolegs, setae) were readily identifiable in theoesophagus 3 hours after consumption of the prey. There is an interestingpossibility that hungry adults in the field may prey upon second-instarbudworm when they leave the hibernaculum in early May. In cages, adultladybeetles were unable to attack the budworm within the hibernaculum, orwithin the mined bud; they were also quite unable to seize the highlyreactive third-instar and older larvae.
Adults in cages also fed on fir pollen and honeydew in June,first-instar crawlers of the scale Agralaspis ithacae (Ferris) in July,Cinara aphids from juniper in August, and artificial diets (basically'beef extract or brewers yeast) throughout the se ason. Smith (1965) notedthat Mulsantina adults were long-lived on diets of banana, casein, or liver.Thus in times of aphid shortage, the adults may have a wide tolerance offood resources,. However, there are limitations; they were unable to feedon the diaspids under the scale, or on beetle mites (e.g. Diapterobates sp.),or any insects which resisted strongly.
Food specificity of larvae
The larva's first meal was apparently the residue in its ownor sibling egg shells, and this appeased its appetite for the first half day.Thereafter, larvae fed upon any unhatched eggs; usually in each clusterone or two eggs were slow to hatch or infertile. On the second day, theyabandoned the cluster and dispersed, foraging for small weak prey.First-instar larvae were unable to seize the larger aphid instars, and therefore
contact with first-instar sexuparae or with sexuals was essential to'survival of very young ladybeetles. Older larvae were increasingly ableto cope with larger prey, including Cinara, and to forage further afield.The ladybeetle larvae did not attack each other unless confined andstarved within a small cage. Larvae ate small aphids completely, butleft most of the exoskeleton of larger aphids, except when starved.Larvae were unable to attack the large budworm and other vigorous insectspresent in June and July.
In cage experiments,the larvae were reared on various diets:living Mindarus, frozen Mindarus, living birch aphids (Betulaphis quadrituberculata (Kelt.), and Calaphis betulaecolens Fitch), and theartificial diets based on beef extract and on yeast as described. The
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effects of these diets on the rates of larval and pupal developmentwere tested by rearings at the quasi-natural temperatures in the insectary(Table 5). Living and frozen M. abietinus aphids were equally acceptableand suitable, but the frozen aphids were the more convenient laboratorymaterial. Frozen aphids have long been known to be suitable for rearingother ladybeetles (Haug, 1938). Njiile Mindarus diets produced long-livedand healthy adults, other diets were generally unsatisfactory; that is,they retarded, the rate of development or did not permit completion of growth.However, it is possible that the failure of larvae to survive on Calaphis aphids was due to starvation rather than to nutritional inadequacy; liveCalaphis nymphs escaped the larvae much more frequently than did Mindarus nymphs.
Table 5. Length of Larval Stadia (Days) of Mulsantina hudsonica Reared onVarious Diets at Natural Temperatures Fluctuating Around a
Mean of 67 F
Diet
Mindarus abietinus Betulaphis Calaphis Beefdiet
Yeastdietlive • liveInstar frozen live
II3.63.9 407
3.78.04.0
5.04.0
6005.0
6.46.3
III 4.1 3.7 5.0 5.0 9.16.4 6.0 11.0
Pupa 8.2 7.7 8.0
Larvaeno. rearedno. completed
development
8
8
3
3
2
1
6
0
1
0
5
0
Daily activity of adults
The more constant features of the daily life of the adult ladybeetleare resting, searching, feeding, and preening.. However the times spent onthese components vary strongly with the passage of the season, particularlyrelative to the needs of reproduction in June. The daily activities werestudied by periods of close observation of several caged individuals on1 day in June, 2 days in July, and 2 days in August.
Resting occupies a large part of each day, and may be expressedin either of two attitudes. In the "sleeping" position, the insect has soughtsome crevice, has withdrawn its legs and does not readily resume activity;this position is adopted by post-reproductive adults during the greaterpart of daylight and also at night. In temporary rest, however, the legsare extended and the insect can be easily provoked to walk or feed.
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In July and. August adults entered long periods of deep rest(partial aestivation) in moist cool shelter, usually for several daysat a time, and were distributed singly or in small groups withoutreference to sex. Caged adults survived as many as 6 summer weeks withoutfood, but died within 1 week denied both food and water. Old adults whichhad overwintered once rested longer and more frequently in July and Augustthan the young adults of the current generation.
Searching activities are motivated by hunger, mating, oviposition,migration,and the need for a resting niche. Searching may occupy severalhours each day in spring, or none at all on some days in summer. Searchingappears to be random with respect to prey, but is clearly photonegativewith respect to shelter.
The act of feeding occupies only a minor part of the adults day,usually less than 1 hour. Feeding takes place mainly in the afternoons,and is apparently inhibited at night. The time to kill and eat an aphidvaries from less than 1 min for a sexual to 9 min for a fourth-instarsexupara. The adult does not kill unless ready to eat but may consumea smaller portion of each individual with increasing satiation. Verysmall prey are eaten entirely, but the exoskeleton of the larger aphidforms is frequently abandoned. The adult attacks small prey from any anglebut usually approaches a large aphid from behind, and seizes it withforelegs and mandibles. It eats with a vigorous chewing motion which causesa fluid oscillation of the prey viscera and is suggestive of salivaryoutflow.
Preening always follows feeding, arid is a cleaning response tothe presence of fragments of prey flesh, wax wool, and honeydew on itsappendages.
The activities of post-reproductive adults on 1 day (2.30 -11.00 p.m. = E hrs on 19 June 1967) were recorded and summarized as anexample of adult behaviour (Table 6). Each of six females was kept ata different constant prey density to determine variation in activityrelative to prey availability. These females were starved for 24 hrs inadvance of the observations, then placed in individual half-pint cageswith fourth-instar sexuparae. The cage temperature followed a naturaltrend from 72 F at 2.30 p.m. to 76 F at 5.15 p.m. to 57 F at 11.00 p.m.
Table 6. Activities of Six Post-reproductive Female Adult LadybeetlesExpressed as Percentage of a Period of 8 1/2 hr of Continuous
Observation
Constant prey density (aphids per cage) ' Activity
3 7 12 20 30 50
I, 1
Resting 64Searching 26Feeding 7Preening 3No. of prey eaten (4)
74
66 62
80
16
14 24
15
8 4 7 9 4
2 ' 1 3 '6 1
(3) (3) (6) (4)
(3)
- 13
The results confirmed the general observation that resting isthe main activity of the post-reproductive adult. Prey density did notappear to affect the amount of time spent searching, or even the numberof prey eaten. Most of the time spent searching was presumably motivatedby a search for dark shelter, since at all prey densities, aphids werefrequently detected and ignored after initial hunger was satisfied.Searching took place at intervals in periods varying from 5 to 60 min, whenthe insect investigated its environs by movements of legs, palps, and antennae.Feeding took place mainly in the early afternoon, but continued sporadicallyuntil dusk. In the last 2 hours (darkness), the insects were observed byfaint light and appeared to be resting. The only relationship betweenactivities was that time in preening was related to time in feeding.
Seasonal voracity of adults
Ladybeetles are effective predators when the number of aphidseaten exceeds the current reproductivity of the aphid. The overwinteredadult ladybeetle has three seasonal phases of voracity:
1. Pre-reproductive phase (May), when prey-searching activity increaseswith warmer weather; at this time aphids are scarce and foodselection is potentially wide.
2. Reproductive phase (June) when mating and oviposition take place;energy requirements are at peak, but so is aphid supply.
3. Summer quiescent phase, when voracity is greatly reduced.
The first of these phases is the most important since it influencesthe density of stem mothers from which later aphid generations will beproduced; and it is the only phase in which the ladybeetle has a potentialinfluence on the spruce budworm. The second phase, the voracity ofreproductive adults, is influential upon the density of sexuparae, eitherdirectly or by further predation upon surviving stet mothers, but aphidreproductivity at this time is usually well in excess of ladybeetle adultcapacity to control it. .The feeding activity of reproductive and post-reproductive adults presumably has very little influence on the arthropodcommunity as a whole.
The rate of food intake of reproductive adults was studiedexperimentally in four chambers at temperatures programmed to 75/60 F,70/60 F, 65/60 F and 60 F constant (see Methods). The feeding experimentwas conducted 28 May - i June 1968; that is, near the supposed peak ofadult voracity. Adults were reared in half-pint containers where preydensity was kept constant at 10 Mindarus stem mothers (adults andfourth-instar nymphs) except on 1-2 June when density decreased with predationand was not maintained.
The results of this feeding experiment (Table 7) show an increasein daily consumption with increase in temperature between 60 F and 75 F.Hagen and Sluss (1966) also reported that ladybeetle adults eat moreaphids under warm conditions. Thus in warm springs, the ladybeetle'sincreased hunting activity tends to counter the aphids faster rate ofreproduction. It is not known whether prey or predator may obtain adifferential advantage with change in temperature. The peak of adult
Table 7. Numbers of M. abietinus Stem Mothers Eaten by Individual Maleand Female Ladybeetle Adults in the Reproductive Phase
Rearing regime
Date 60 F 65/60 F 70/60F 75/60 F
d d d 2 2 2 Q 2 d cr
28 May 4 8 6 7 8 3 i0 8 3 3 3 6 3 6 5 529 5 6 5 6 9 9 14 7 11 7 11 18 13 12 18 1430 4_ 1 6 a 6 6 i4 8 6 ,i;. 12---20 5 2 10 631 5 11 7 13 9 11 11 u 9 12 14 15 9 9 16 10
1-2 June 6 5 0 6 0 3 0 - 6r 3 - 3 3 0 2 4 6 53 11 6 l0 l0 9 16 18 10 11 11 16 10 9 19 244 8 8 2 4
7 5 17 14 5 7 12 17 6 16 17 20
Total 43 45 36 54 46 46 93 72 47 47 66 92 48 58 91 84
Mean con-sumptionaphids/day
5.4 5.6 4.5 6.7 5.7 5.7 11.6 9.0 5.9 5.9 8.2 11.5 6.0 7.2 11.4 10.5
Daily con-sumption(mg) liveweight
1.6 1.7 1.3 2.0 1.7 1.7 3.4 2.7 1.8 1.8 2 .5 3.4 1.8 2.2 3.4 3.1
Ladybeetleadult weight(mg)
8.4 7.7 6.1 11.5 8.8 8.5 8.9 9.8 6.5 5.4 11.6 11.6 8.4 8.4 10.6 8.9
Eggs perperiod
- - 4 10 0 0 16 - 0
- 15
feeding may be reached 'early in June in the average year, and maximumconsumption may be around 3 mg/day of live weight of aphid for femaleladybeetles, and 2 mg/day for males. The table shows that the experi-mental females were heavier (mean 10.0 mg) than the experimental "males(mean 7.3 mg). Thus consumption may be a function of body weightrather than of sex.
In another experiment, in which six males and eight females wereprovided fourth-instar elate aphids over a 5-day period 'l1-15 June 1968) atinsectary temperatures (mean 59 F), adult consumption was 0.8 mg/day forfemales and 0,7 mg for males. However, it is not known how much suchmeasures of prey consumption may be conditioned by confinement in cages,by prey density, and by experimental handling.
No quantitative studies of food consumption by adults of the currentyear's brood were undertaken, but it was observed that teneral adults onbalsam fir fed actively so long as the aphid sexuals persisted in July, andsuch feeding in the first week or ,so of adult life is probably necessary toaccumulate fat reserves, Feeding by the earliest new adults could reduce thedeposition of eggs by the last-surviving Mindarus sexuals, more especially onspruce, but such predation would be only a minor factor in the aphidpopulation mortality. There is no doubt that the voracity, of overwinteredadults in spring is much greater and has much more effect on the preypopulation dynamics than the voracity of the adults of the new generationin summer,
Voracity of larvae
Whereas adult feeding tends to be sporadic and interspersed withrest) periods, larval activity is more continuously motivated by hunger.Larvae search the foliage for prey throughout daylight, except when theyare cold, fully sated, or approaching ecdysis. Larval appetite is large;in one experiment, a newly moulted fourth-instar was starved for 2 daysthen fed a succession of adult female sexual aphids; it consumed 35 aphidsin 65 min when satiation was reached, The intake of prey in this singlemeal was 1.19 mg, and the weight of the larva increased from 2.75 mg to3,94 mg, and its length from 3.75 to 6.00 mm in little more than 1 hour.
An experiment was conducted to test the effect Of temperature onfood intake, Larvae were reared from the first-instar at the four temper-ature regimes (60 F const., 65/60 F, 706o F, 75/60 F), Prey density wasintended to be maintained constant at 12 female sexuals (third-instar,fourth-instar, and adult) of M. abietinus, but in practice its maintenancethroughout the fourth stadium of the ladybeetle larvae proved too onerous,Thus the larvae in the warmer regimes (75/60 F and 70/60 F) completed theirdevelopment in semi-starvation due to inadequate maintenance of prey density.On the other hand, larvae in the cooler regimes (65/60 F, 60F constant)completed their growth on a substitute diet, the much larger fourth-instarsexuparae of M. abietinus, The attempt to equalize prey density in alltemperature regimes was therefore not fully achieved,
Table 8. Food Consumption and Stadial Durations of 14 Larvae of Mulsantina hudsonicain 4 Temperature Regimes
Item Rearing regime
60 F const. 65/60 F 70/60 F 75/60 F
Second stadium
No. of days 4 4 4 5 4 5 3 3 3 3 3 3 3 3No. of sexuals eaten 37 18 40 30 16 44 19 36 33 27 23 30 25 22Hg prey eaten 1.4 .7 1.5 1.1 .6 1.6 .7 1.3 1.2 1.0 .9 1.1 .9 .8
Third stadium
No. of days 7 4 8 6 5 5 5 4 4 4 3 5 3 3No. of sexuals eaten 66 42 64 49 55 56 75 48 54 54 59 52 -58 60
prey eaten 2.4 1.6 -2.4 1.8 2.0 2.0 2.8 1.8 2.0 2.0 2.2 1.9 2.1 2.2
Fourth stadium
No. of days 12 13 11 11 11 10 12 9 9 8 9 10 8 8No. of sexuals eaten 65 106 73 41 67 75 69 111 136 92 136 103 99 122No. of alates eaten. 12 10 11 12 11 12 12 0 0 1 0 8 0 0Mg prey eaten 7.8 8.4 7.6 6.9 7.3 8.2 7.9 4.1 5.0 3.9 5.0 7.4 3.7 4.5
Totals
No. of days 23 21 23 22 _ 20 20 20 16 16 15 15 18 14 14Mg prey eaten 11.6 10.7 11.5 9.8 9.9 11.8 11.4 7.2 8.2 6.9 8.1 10.4 6.7 7.5
- 17
Nevertheless the results (Table 9) gave some information onthe rate of food intake by successive instars, on total larval consumptionand on the rate of larval development at various temperatures.
The daily rates of food intake (in mg) by larvae are calculatedfrom Table 9 as follows:
Instar
Rearing regime
60 F const. 65/60 F 70/60 F 75/60 F
Second 0.27 0.24 0.37 0.31Third .33 .46 .48 .60Fourth .66 .64 .50 .58
These means show increasing consumption with temperature in thesecond and third stadia, but the expected projection of this trend in thefourth stadium was prevented by the starvation that prevailed in the twowarmer regimes. Constant prey density was more nearly attained in the twocooler regimes, and mean daily consumption increased in successive instars.It is possible that under conditions of unlimited food supply (not improbablein a year of high Mindarus abundance) the increase in daily food consumptionfrom instar to instar would be in geometric progression, A reasonableestimate of the average live weight of prey consumed in the field would beas follows:
InstarConsumption
II
CIII
Iv
Total
Mg/day
0.2
0.3
0.5
1.0Mg/stadium .4
1.1
2.0
7.0
10.5
These values exclude the weight of diet (sibling eggs) consumed by thefirst-instar in the first 2 days.
The largest individual food consumption (recorded from rearingsat quasi-natural temperatures in the insectary) was 13.4 mg live weightof aphids. No experiments were conducted to determine the relationship oflarval food consumption to aphid density, but a positive correlation withinlimits could be expected (Hodek, 1967). Even after the plateau of maximaldaily ingestion is reached, the rate of aphid kill could continue to increasebecause ladybeetles eat less of each individual with increasing ease ofcapture,
Relationshi betwee ood intake b larvae and subs e uent, size of adults
Table 8 shows the weights of prey consumed by 14 larvae throughstadia II to IV. These same individuals were then weighed as living
18
teneral adults before resuming feeding, and measured to length and headwidth (Table 9). The weight of food ingested by the larva is directlyrelated to the weight and body dimensions of the adult subsequentlyreared (Fig. 2a, b ). This suggests that after a spring when aphids
are scarce, the population of summer adult ladybeetles will be smallerboth in absolute numbers and in mean individual size.
Table 9. Relationship Between Food Consumption by Larvae ofM. hudsonica and Subsequent Adult Size and Weight
Rearing Food consumed Live weight Lengthregime by larva in of adult of adult
stadia II-IV (mg) (mm)(mg)
Headwidth(mm)
Sizeindex(LXW)
60 F const. 11.6 9.4
4.6
1.1
5.1
11.5 7.3
403
1.1
4.7
9.8
4.3
1.1
4.7
65/60 F 9.9 7.3 4.3 1.2 5.2
11.8 7.5 4.1 1.2 4.9
11.4 10.4 4.5 1. 5.8
70/60 F 7.2 6.6 4.0 1.0 4.04.2 6.5 4.0 1.1 4.4
6.9 6.2 3.9 1.1 4.3
75/60 F 8.110.46.77.5
6.38,44.65.5
4 .2,4.43.73.8
4.65.33.74.2
The dimensions of adult body length and head width should becorrelated with their past history of food consumption as larvae (Fig. 2b).Thus in the laboratory collection of 270 field-collected adult Mulsantina hudsonica, the largest individual has a size index of 6.5 (body length 5.0mm x head width 1.3 mm) and the smallest individual has an index of 3.8(body length 3.8 mm x head width 1.0 mm.) These values should relate tolarval consumptions of 16.2 mg and 5.7 mg of live aphids, if a straightline relationship obtains in Fig. 2 b. It can also be assumed that larvaefailing to obtain this minimal weight of food, would fail to mature.
It is possible that the smallest adults do not survive long.Dixon (1959) related Adalia decempunctata (L.) larval consumption of foodto the size and weight of adults, but noted that field populations didnot include individuals as small as those he was able to rear by partialstarvation. He suggested that there might be a selective mortality ofundersized teneral adults.
B
LL0 12
10
8
7
E
12
10
5 6 7 8 9 10
WEIGHT OF ADULT (mg)0
5 6
SIZE INDEX OF ADULT
Figure 2. Relationship between consumption of Mindarus aphidsby Mulsantina larvae and subsequent adult size in
(A) weight, and (B) dimensions (body length x headwidth).
-19
The ability of ladybeetle larvae to develop in spite of areduced food supply may be very influential upon the population dynamicsof that species. A species with a large sexual difference in the weightand size of adults may respond to an increasing food supply by a largerratio of females to males, i.e. higher survival of female larvae whenfood is abundant compared with when it is scarce (Smith,1966). Onthe other hand, the sex ratio of a species witi small size differencesbetween sexes does not change much with changing prey density. Onthis reasoning, therefore, Mulsantina hudsonica would be less capable ofa rapid numerical response to changing prey density than some otherladybeetles, such as Anatis mali auct.
Other coccinellid species on fir
Mulsantina hudsonica is by far the most abundant ladybeetle onbalsam fire Other species collected as adults were Anatis mali, Adalia bipunctata L., A. frigida (Sohn.), Coccinella monticola Mule., Chilocorus stigma Say., and Coccinella transersoguttata Fald. Species collectedas larvae were M. hudsonica, A. mali, A . bipunctata, and C. stigma. Itis not known whether there is interspecific competition for the Mindarus aphids on fir and spruce, but it is perhaps surprising that one coccinellidspecies should dominate this major food resource in so extensive anecosystem. The food specificity of the other coccinellids present in firstands is little known, but gut dissections of C. stigma adults and larvaehave revealed fragments of the fir-dwelling scale insect Agralaspis ithacae (Ferris) but none of aphids. In this instance, therefore, Chilochorus was not competing with Mulsantina although occupying the same habitat.Similarly Cinara has been found in the oesophagus of A. mali larvae. Thusit is possible that food-specificity limits interspecific competition.
POPULATION RELATIONSHIPS BETWEEN MULSANTINA HUDSONICA AND MINDARUS ABIETINUS
Synchronism of life cycles, and comparison of population densities
Close synchronism of the life cycles of a sedentary prey speciesand its specific coccinellid predator is usual (Hagen, 1962), and theMindarus Mulsantina relationship is no exception. Indeed, this synchronismcan be expected to be very well balanced since the spruce-fir habitat isa very stable one compared with the agricultural ecosystems occupied bythe economically important species of ladybeetles. Compared with agriculturalpest aphids, perennial populations of M. abietinus appear to be quite stablein spite of a mild, oscillation with an interval of 4 to 5 years betweenpeaks (Varty, 1968). However, aphid and ladybeetle populations have beenquantitatively assessed only in 1966 and 1967, so only a start has been madein comparing perennial densities. For real advances in the study ofbiological control, there is a need for long-term studies of non-pestaphids in undisturbed areas (Hagen and Van den Bosch, 1968).
Mindarus abietinus is multivoltine with a characteristic pop-ulation trend (Fig. 3) modified mainly by the seasonal abundance orscarcity of the fecund fundatrigenia morph (Varty, 1968). The abundanceof the aphid rises as the egg hatch in May, next declines as the firstgeneration suffers mortality, then rises very rapidly to high density in
1 04
03
U
4
NI-0
102
4U.0wm2Z 10
NUMBER OF APHIDS
WEIGHT OF APHIDS
• 10
10
N
0
9n.4
• o
0w3
200 400 600 800 1000
1200
1400 1600DEGREE - DAYS
Figure 3. Seasonal progression in 1966 of B-level population ofMindarus abietinus from balsam fir at Lincoln, nevertreated with insecticide. Comparison of aphid densityexpressed as numbers and as milligrams per 10 ft 2 ofbranch surface.
Degree days Mindarus abietinus
100
Stem mother larvae hatch.(early Mayat Fredericton)
300(late May)
400-700(early-mid June)
500 Abundant early-instarsexuparae in colonies.
Rapid climb in biomassFirst sexuparae born.
Biomass high and rising,due to birth of sexuparae.
-20
June as second, third, and fourth generations succeed one another, andfinally diminishes in early July when the sexuals produce eggs and die.However, as far as predation is concerned, weight of prey rather than thenumber of individuals is more important. The graph of seasonal aphid biomass(Lincoln plot in 1966) is compared with the graph of seasonal numbers; biomasskeeps on increasing from the beginning of the season and peaks more abruptlybefore declining. Thus the use of biomass shows an earlier and somewhatnarrower season of aphid abundance compared with the use of numbers ofindividuals (Fig. 3).
The synchronism of the univoltine cycle of the ladybeetle and themutivoltine cycle of the aphid can be conveniently compared in terms ofaccumulated degree-days (Fig. 7) referable to all plots, as follows:-
Mulsantina hudsonica
Adults begin feeding onstem mothers.
Increasing voracity toprepare for oviposition.
Oviposition period. Intenseadult feeding.
First-hatching larvae begin,to feed on early-instaraphids.
700(mid June)
900(late June)
1500(late July)
Peak biomass, sexuparaestill in colonies.
Peak numerical density ofsexuals, i.e. maximum numberof contacts between prey andpredator. Distribution morerandom, less colonial.
No aphids
Maximum numbers of younglarvae.
Peak larval biomass i.e.peak consumption of aphids.Larvae older, more able toforage, less dependent uponcolonial association of prey.
First pupae. Most larvaenow late-instar.
Larval biomass near zero.Teneral adults feeding.
Hungry young adults migrateto spruce.
1000 Biomass still high but rapidly(early July) declining.
1300 Biomass near zero(mid July) (only sexuals remain)
Mindarus abietinus is available as. food usually between 100 and1400% with peak biomass around 700°D. The early portion of the food supply isused by overwintered adult ladybeetles to prepare for and sustain oviposition.The ladybeetle larvae hatch between 500 and 700°D in the midst of an
- 21
abundant food supply. Each larva develops through its four larvalstadia in approximately 475 D. The density of prey biomass diminishesgradually as the larvae develop, but the older larvae can forage furtherand the frequency of encounter with aphids remains high. Towards theend of the larval phase, prey becomes scarce and competition for foodgreater, so that after 1000 D there is a risk of larval starvation.Starvation must vary year by year, from locale to locale, and from treeto tree according to (1) prey biomass density and its rate of decline, (2)the foraging capacity of the larva by instar, and (3) the intensity ofinterspecific competition for currently available prey. It can bespeculated that starvation may be the rule after 1200 D (aphid biomassless than 5 mg/lOft ) resulting in death of larvae and pupae, and thiscould account for the parallelism of the declining curves of prey andpredator biomass in some plots (Fig. 4a, b; 5a). The closer the proximityof these curves, the stronger will be the competition among predatorylarvae and the greater the density-dependency of survival.
It is reasonable to suppose that there will be a series of preydensity thresholds for survival of the four ladybeetle larval instars.Therefore when prey biomass is low throughout the season, as at GreenRiver in 1967 (Fig. 5b), there will be curtailment of larval survival inSpite of a high aphid-ladybeetle ratio. Under such circumstances, theproblem is not one of competition for food, but of dispersal of preywith respect to the larva's searching capacity. Only the contagiousdistribution of aphid populations, or the presence of a buffer food resource,prevents local extinction of the ladybeetle. The prospect of larvalstarvation may be tempered by the presence of alternative prey around1200 D, such as thrips or Cinara aphids, but the effectiveness of suchbuffers has not been investigated. Some such mechanism may account forthe continued survival of the ladybeetle at Priceville, where populationsof M. abietinus are disproportionately low (Fig. 6).
The effectiveness of M. hudsonica in regulating populationdensity of M. abietinus has not yet been quantitatively assessed. Thisladybeetle qualifies as a "good" predator as specified by Hodek (1967)because (1) it has a high searching activity, (2) it occupies all thehabitats of the aphid, and (3) its adult weight is adjustable to foodscarcity. Factors such as its ability to survive adverse conditions andthe incidence of enemy organisms are unknown. Its effect as a predatormust be exercised mainly against the first aphid generation before 250(when the aphid starts to reproduce) and the last generation after 1000 D(when aphid eggs are being laid). However, the ladybeetle may have littleeffect upon the surge of aphid population between 300 D and 700 D, whenthe aphid's rapid development and high fecundity far outweigh theladybeetle's appetite. The aphid population at peak level may be regulatedin large measure by flight dispersal of the alate adults, a non-densitydependent mortality factor.
The direct density-dependent relationship between the ladybeetleand the aphid is both immediate and delayed. A high biomass of prey willtend to encourage high survival of ladybeetle larvae, and thereforea heavy mortality of sexuals before they can deposit eggs. Moreover,
02
10
I0
0.I200 400 600 800 1000
1200
103
DEGREE - DAYS
Figure 4. Comparison of seasonal changes in biomass for Mindarus aphids andMulsantina larvae in 1966 and 1967 at (A) Lincoln, never sprayed, and(B) Penniac sprayed with Phosphamidon in 1966 but untreated in 1967,.
10
CV
01
E 1°3
102
IO
0.1
j0
SPRAY SPRAY1966 1966
1102
Mindorus obietinus
.1.--
//
/ 1I 1
/ 1/
%IMulsonlino hudsonico ■%
I%
1t
II
s It
I t
I II
1
tI
t I
t 1
200 400 600 800 1000 1200
Mindorus obiefinus
Mulsantino hudsonico
DEGREE - DAYS
Figure 5. Comparison of seasonal changes in biomass for Mindarus aphids and Mulsantina larvae at (A) Killarney, sprayedwith DDT in 1966, and (B) Green River untreated, in 1967,
Mulsontina hudsonica1967
102
w
zrr 10
NLL
O
E
03
LTJ
w
zz
200
400
600 800
1000
12 00
DEGREE - DAYS
Figure. 6. Comparison of seasonal changes in biomass forMindarus aphids and Mulsantina larvae in 1967at Priceville, sprayed annually (1958-1967)with DDT.
-22
the new summer generation of ladybeetle adults will be of large averagesize and great potential fecundity. The ,net effect will be a larger,more vigorous population of adults next spring ready to prey on thehatching aphids. Conversely a low biomass of prey should tend to depressladybeetle survival and the size of new adults, resulting in reducedpressure on the aphid next season. This mechanism could partly accountfor the low amplitude of Mindarus populations oscillation. Measurementsof prey and predator biomasses over 4 to 5 years should demonstrate whethera simple bilateral density-dependence dominates the relationship betweenMindarus and. Mulsantina populations. The evidence available from theunsprayed plot at Lincoln in 1966. and 1967 (Fig. 4a),is too limited forsuch interpretation.
The effect of insecticides on prey-predator relationships
The densities of aphid biomass in three plots near Fredericton(Fig. 5a, b; 6a) followed similar seasonal trends in 1966 in spite ofdissimilar measures of insecticide control: untreated (Lincoln), Phosphamidon(Penniac), and DDT (Killarney). Clearly the insecticides had no disastrouseffect upon M. abietinus, but nevertheless there are differences in therates of change of density. Whereas the aphid curves in the untreatedplot (Fig. 4a) and in the Phosphamidon plot (Fig. 4b) show steep and almostparallel rates of increment, the curve in the DDT plot (Fig. 5a) rises muchmore gently after 500 D (i.e. post-spray). In the same season, ladybeetlelarval biomass (1) in the untreated plot increased at moderate steepnessto a moderate peak (3.5 mg/10 ft1, 2 (2) in the Phosphamidon plot increasedweakly to a low peak (0.4 mg/10 ft ),,and in the DDT plot increasedvery steeply to a high peak (19.0 mg/10 ft ). Thus there were markeddifferences in levels of ladybeetle density in response to rather similar,high levels Of prey; that is, the ladybeetle biomass in the DDT plot wasalmost 50 times greater than in the Phosphamidon plot. It is temptingto ascribe this variation to differential effects of insecticide. ft isplausible to suppose that the use of DDT actually enhanced survival ofMulsantina larvae, possibly by a selectively toxic effect en the enemyOrganisms attacking ladybeetle eggs and larvae. The phenomenon of lady-beetle increase in DDT-sprayed fir forest has been noted several times(Macdonald and Webb, 1963). Moreover the variance in aphid populationsfrom branch samples in the DDT plot was much greater than the varianceof populations in the untreated plot at similar mean densities (Varty,1968). This means that sample branches in the treated plot containedless uniform numbers of aphids than in the untreated plot. The greaterirregularity of the aphid distribution in the treated plot could beinterpreted as a consequence of the spotty distribution (sibling groups)of abundant ladybeetle larvae feeding heavily on, some branches but noton others. The greater uniformity of aphid tallies in the untreated plotcould result from the relative scarcity of ladybeetle larvae causinglocal mortality of aphids on particular branches.
In the plot with a perennial history of DDT sprays (Priceville),sampling in 1967 indicated a low aphid density with an early peak at600 D, and a surprisingly high density of ladybeetle larvae, (peak at
-23
3 mg/10 ft2 at 1000°D.) (Fig. 6). The predator density was therefore
greatly out of balance with the density of M. abietinus, if indeedsampling precision is adequate at such low density. It is possible thatCinara abieticola, found frequently in the digestive tracts of adultladybeetles in this plot, may also provide an alternative diet forMulsantina larvae.
In the Phosphamidon plot (Penniac 1966), the biomass curves forladybeetle and aphid suggest that ladybeetle survival was depressed whileaphid survival was unaffected. In the spray year 1966, the increment ofladybeetle larval biomass increased slowly to a low and early peak, 0.4mg/10 ft at 700 D (Fig. 4b). This could be interpreted in various ways:as the effect of a very low initial population of parent beetles; asevidence of the failure of adults to lay the full complement of eggs, oras evidence of the failure of larvae to develop beyond the early instars.The first spray (370 D) could have affected the pre-reproductive adultladybeetle population, while the second (590 D) could have affectedovipositing females and first-instar larvae; this assumes, of course, thatPhosphamidon could act as a contact insecticide soon after application.
In the following year, 1967, no insecticide was sprayed in thePhosphamidon plot, and ladybeetle biomass was similar to that in theuntreated plot (Lincoln) in the same year. The recovery of the ladybeetlepopulation was a rapid density-dependent response to the aphid food resourcewhen insecticide stress was removed from the system.
It is instructive to compare the densities of ladybeetle andaphid at the peak of the formers seasonal abundance (Table 10). The twoDDT plots (Killarney in 1966 and Priceville in 1967) show a low ratio ofprey to predator numbers, i.e. it is presumed that ladybeetles contributedeffectively to the regulation of aphid populations in both these plots.The Phosphamidon plot, in contrast, showed a high ratio in the year ofspray, i.e. poor numerical response by the predator. One other location,the unsprayed plot at Green River, also showed a high ratio, presumablybecause the early decline in aphid biomass caused starvation of manyladybeetle larvae. Compare the short season of aphid biomass at GreenRiver (Fig. 5b) with the long season of aphid biomass at Fredericton(Figs. 4a, b; 5a). In both these instances of high ratio, the peak ofladybeetle larval biomass occurred early, around 700 D, suggesting thepoor survival of newly hatched ladybeetles. Plots with high prey densityand no treatment with insecticide, showed intermediate aphid-ladybeetleratios, as well as a steep increment of larval biomass with peaks at900 to 1000 D; provisionally this is considered to be the "normal"relationship between well-established populations of M. abietinus andM. hudsonica. However, a longer history of population estimates and awider series of insecticide stress situations, together with someexperimental assays, are needed to arrive at any firm conclusions uponthe effect of chemical treatment on this biological system.
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Table 10. Relationship Between Density of M. hudsonica Larvae, Density ofM. abietinus Prey, and Insecticide Application
Insecticidetreatment
Year M. hudsonica peakdensity of larvae
o / 2at D mg/10 ft
M. abietinus Ratioaphid/lady-beetle
Plotlocationcorresponding
density mg/loft
DDT 1966 900 19.0 25 1.3 KillarneyDDT 1967 .1000 2.9 1 .3 PricevillePhosphamidon 1966 700 .4 100 250.0 PenniacNil 1967 900 2.3 8 3.5 PenniacNil 1966 1000 3.5 22 6.3 LincolnNil 1967 900 4.8 15 3.2 LincolnNil 1967 700 .5 21 42.0 Green River
A comment on sampling problems
The sampling method was designed to estimate populations of ,the aphidM. abietinus on B-level branches from which a positive count was almostinvariably obtained. However, the numbers of ladybeetle larvae were far mailerand even at the most favourable part of the season only a small proportionof positive samples was obtained from each lot of 40 branches (Table 11).Positive samples were obtained only between 597 D and 1180 D, as would beexpected from the seasonal history, and the peak proportion of positive samplestended to be around 900
oD. The data are inadequate to show any expected
increase in density (larvae per branch) with increase in the proportion ofpositive samples. The table merely indicates that larvae are widely dispersedand rarely occur in groups.
This pattern of distribution is similar to that obtained by Miller(1964), sampling endemic populations of spruce budworm in New Brunswick, andusing the same sampling unit, one B-level branch per tree. His data showedthat with 0.4 budworm larvae per branch, 736 trees would be required to bringaccuracy within a sampling error of 20%. Since Mulsantina larval densityrarely exceeds 0.4 per branch, it would be beyond the scope of this researchto seek such accuracy. The plot-date (Killarney, 30 June 1966) of highestmean density recorded, 0.58 larvae per branch, showed a standard deviationof 0,84, and a coefficient of variation of 147%. Other plot-dates of lowermean showed, even greater variability in distribution. Thus the estimates ofladybeetle, larval density are statistically unreliable. However, grossdifferences between plots across a seasonal trend, repeated in successiveyears, are undoubtedly real, and it is considered reasonable to look formajor changes in ladybeetle density in response to changes in prey densityand insecticidal treatment. However, inferences based on these measurementsshould be supported by a better knowledge of between-level distribution.
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Table 11. Frequency of Occurrence of Mulsantina hudsonica Larvae on B-Level Sample Branches of Balsam Fir in 1966 and 1967
Degree-days
Date Plot Areaof branch
samples (ft2)
arvae per branch
0 1 2 3 4 5
1966
600 13 June Lincoln 115 37a 2 100 0620 14 June Killarney 118 35 2 0 0 1630 16 June Penniac 135 34 5 1 0 0 0760 21 June Lincoln 123 35 5 0 0 0 0780 22 June Killarney 98 31 5 3 0 0 1920 28 June Lincoln 128 34 6 0000930 29 June Penniac 106 38, 2 0 0 0 0975 30 June Killarney 94 25 8 6 1 0 0
1090 5 July Lincoln 110 35 5 0 0 0 01100 6 July Killarney 92* 32 6 . 0 2 0 0
1967597 19 June Lincoln 86 37 1 1 1 0 0605 20 June Penniac 88 39 0 1 0 0 0692 5 July Green River 123 38 2 0 0 0 0789 10 July Green River 127 39 0 1 0 0 0873 7 July Priceville 94 38 2 0 0 0 0948 5 July Lincoln 90 33 7 0 0 0 0969 6 July Penniac 97 36 4 0 0 0 0
1039 14 July Priceville 101 36 4 0 0 0 01157 13 July Lincoln 122 38 2 0 0 0 01180 27 July Green River 96 38 2 0 0 0 0
708 70 16 40 2.
aNumber of samples out of 40.
DISCUSSION
A. series of studies on the predaceous insects and spiders ofthe spruce-fir forest has been conducted in the Maritime Provinces byvarious research scientists in the past two decades. These studies havebeen aimed at determining the influence of these predators upon a fewspecific pests, notably the spruce budworm and the balsam woolly aphid.The investigations have been partially successful in identifying some ofthe predators present on balsam fir, but they have not culminated in aquantitative assessment of the ecological impact of these predators onforest productivity. A knowledge of the ecological niche of the predatorsof the major pests and a demonstration of their numerical and functionalresponses to major prey, that is, the control value of predators, is stillneeded.
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I submit that such relationships are not readily demonstrablebecause the spruce budworm and the balsam woolly aphid form only a veryminor part of the food resources of the predator complex. The sprucebudworm occurs at very low density except during periodic outbreaks; soit is unlikely that a close behavioural relationship between any predatorand a low-biomass prey could have evolved, or that a predator's numericalresponse to the erratic prey resurgence could be other than limited.Similarly the balsam woolly aphid is an alien species introduced only 60years ago. There can be no question of evolved response by native predatorsto the balsam woolly aphid, only a secondary adaptation from their responsesto native adelgids.
This argument, however, does not conflict with my original contentionthat predators should be studied to assess their ecological impact. It ishighly probable that if non-specific predators can be maintained at a highlevel of abundance, then their foraging activity - casual feeding on a widespectrum of prey - will dampen the oscillation of major pests so long asthose pests are at a low level of abundance, It is possible that non-specific predatory activity will thus help to maintain the spruce budwormand the balsam woolly aphid below epidemic levels. If this is so, then thefactors, density-dependent and physical, which influence the density andstability of the predators, should be appreciated so that , we do not blunderinto undermining their position by blind application of pest controlmeasures.
1
The example of Mulsantina hudsonica is very much to the point.We have seen that it could be a potent predator on the budworm only inearly spring, at the time when the young budworm larva emerges from itshibernaculum. But if a large population of hungry ladybeetle adults occupiesthe same habitat as a small population of migrating budworm larvae, thereis a prospect of significant pest mortality. Similarly it is possible thatthis ladybeetle affects the abundance and distribution of balsam woollyaphid in the crowns of firs, assisting other regulative processes. Thisladybeetle may be part of the predatory complex which prevents otherphytophagous insects from attaining pest status. Thus the interaction ofladybeetle, prey and insecticide is one of potential importance.
Finally Mulsantina hudsonica is an example, probably a typicalone, of an arboreal ladybeetle of the northern coniferous forest in anold and stable ecosystem. Of hundreds of papers on Coccinellidae, veryfew deal with species restricted to the coniferous habitats (Klausnitzer,1966). Most other studies have been concerned with various ladybeetlesin the, modified habitats of field and orchard culture, and the abundanceand survival Of these species reflects their genetic heterogeneity andecological plasticity. It remains to be keen whether M. hudsonica canexhibit such qualities if we cohtinue to modify its habitat.
1
SUMMARY
Mulsantina hudsonica Casey is a small brown coccinellid restrictedto the spruce-fir forest but abundant in New Bru nswick. It is a strictlyunivoltine species of relatively low fecundity. It mates and reproduces
in spring, and larvae develop in June and July. Immature adults foragelightly in summer and autumn, and'probably hibernate in the litter.
All stages feed mainly on the balsam twig aphid Mindarus abietinus Koch, but other insects, honeydew, and some vegetative materials are also'ingested. It can be reared with partial success on artificial diets.An adult may eat 2 to 3 mg/day live weight of aphid at the peak of itsvoracity (in the ovipositional period), and a larva usually eats morethan 10 mg during its four stadia (around 3 Weeks). The amount of foodeaten by the larva determines the size and weight of the adult.
The life cycle of the ladybeetle is closely synchronizedwith the life cycle of the aphid. The biomasses of the aphid and ofthe ladybeetle larvae have been plotted over a degree-day scale; it isevident that the adult ladybeetles use the early-season prey biomass asa food resource sustaining oviposition, while their larval offspringmake use of the late-season prey biomass. There is some evidence of adensity-dependent relationship of ladybeetle populations to aphid populations.Predation by adult ladybeetles in May has a marked influence on the seasonallevel Of the aphids density, but it rarely alters the pattern of aphidpopulation increment; that is, the rate of aphid reproduction is suchthat ladybeetle adult and larval predatory responses together are unableto control the characteristic burgeoning of the aphid population in June.'When prey density collapses due to dispersal of winged aphids, the ladybeetlelarvae are again able to exert an influence on the survival of the lastgeneration of aphids, and therefore upon the deposition of overwinteringaphid eggs. However, the numerical and functional responses of the ladybeetleto the aphid remain largely unexplored.
Tallies of populations of ladybeetles and aphids in plots subjectedto insecticide treatment, have led to the interim conclusions that DDT maypromote the effectiveness of ladybeetle predation upon the aphid, butin long term reduces the absolute populations of each. Phosphamidon,on the other hand, may reduce both effectiveness and survival of theladybeetle. These studies are important in indicating the effect ofinsecticides on non-target insects in a budworm-dominated system, and indetermining 'population interactions in the fir community with or withoutchemical manipulation.
MAY
1
4 11 18 25 I 8 15 22 29 5
JUNE
12 19 26
JULY
Figure Accumulation of degree-days (from base 42F) against date showingthat (1) spring was warmer and earlier in the order Fredericton(south-central region of LB.), Priceville (central) and GreenRiver (northern), and (2) May was much warmer in 1966 than in1967 at Fredericton.
200
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Hagen, K. S. 1962. Biology and ecology of predaceous Coccinellidae. Annu.Rev. Entomol. 7: 289-326.
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